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Phylogenetic Studies of Pantherine Cats (Felidae) Based on Multiple Genes, with Novel Application of Nuclear -Wbrinogen Intron 7 to Carnivores

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Phylogenetic Studies of Pantherine Cats (Felidae) Based on Multiple Genes, with Novel Application of Nuclear -Wbrinogen Intron 7 to Carnivores Molecular Phylogenetics and Evolution 35 (2005) 483–495 www.elsevier.com/locate/ympev Phylogenetic studies of pantherine cats (Felidae) based on multiple genes, with novel application of nuclear -Wbrinogen intron 7 to carnivores Li Yu a,b,c, Ya-ping Zhang a,b,¤ a Laboratory of Cellular and Molecular Evolution, and Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China b Laboratory for Conservation and Utilization of Bio-Resource, Yunnan University, Kunming 650091, China c Graduate School, Chinese Academy of Sciences, Beijing, China Received 14 July 2004; revised 16 January 2005 Abstract The pantherine lineage of the cat family Felidae (order: Carnivora) includes Wve big cats of genus Panthera and a great many mid- sized cats known worldwide. Presumably because of their recent and rapid radiation, the evolutionary relationship among panthe- rines remains ambiguous. We provide an independent assessment of the evolutionary history of pantherine lineage using two complete mitochondrial (mt) genes (ND2 and ND4) and the nuclear -Wbrinogen intron 7 gene, whose utility in carnivoran phylog- eny was Wrst explored. The available four mt (ND5, cytb, 12S, and 16SrRNA) and two nuclear (IRBP and TTR) sequence loci were also combined to reconstruct phylogeny of 14 closely related cat species. Our analyses of combined mt data (six genes; t3750 bp) and combined mt and nuclear data (nine genes; t6500 bp) obtained identical tree topologies, which were well-resolved and strongly sup- ported for almost all nodes. Monophyly of Panthera genus in pantherine lineage was conWrmed and interspeciWc aYnities within this genus revealed a novel branching pattern, with P. tigris diverging Wrst in Panthera genus, followed by P. onca, P. leo, and last two sis- ter species P. pardus and P. uncia. In addition, close association of Neofelis nebulosa to Panthera, the phylogenetic redeWnition of Otocolobus manul within the domestic cat group, and the relatedness of Acinonyx jubatus and Puma concolor were all important Wnd- ings in the resulting phylogenies. The potential utilities of nine diVerent genes for phylogenetic resolution of closely related panther- ine species were also evaluated, with special interest in that of the novel nuclear -Wbrinogen intron 7. 2005 Elsevier Inc. All rights reserved. Keywords: -Fibrinogen intron; Pantherine lineage; Felidae; Phylogenetic analysis 1. Introduction The pantherine lineage, as the most recently evolved (within 1–8 MYA; Janczewski et al., 1995; Pecon Slat- The Felidae, or cat family, is characterized by recent tery et al., 1994) and largest felid group (around 20 cat bursts of diversiWcation within the last 10–15 million species; Janczewski et al., 1995) has demonstrated great years (Johnson and O’Brien, 1997; Martin, 1980; confusion in their taxonomy and phylogeny. These Nowak, 1999; Werdelin, 1985). Thirty-eight cat species pantherine cats consist of Wve big cats of genus Panthera of this family are generally divided into the pantherine, and a great many midsized cats species. They had been domestic cat, and ocelot lineages (Ewer, 1973; Janczew- disputably assigned to 2–13 genera under various classi- ski et al., 1995; Leyhausen, 1979; Masuda et al., 1996). Wcation schemes in past studies (Ewer, 1973; Hemmer, 1978; Leyhausen, 1979; Nowak, 1999) and moreover, ¤ Corresponding author. Fax: +86 871 5195430. phylogenetic relationships among these pantherine spe- E-mail address: [email protected] (Y.-p. Zhang). cies have also been controversial. 1055-7903/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2005.01.017 484 L. Yu, Y.-p. Zhang / Molecular Phylogenetics and Evolution 35 (2005) 483–495 A wealth of molecular characters have been used to elis temminckii (Asiatic golden cat), Prionailurus bengal- decipher feline evolutionary history, including protein ensis (Asiatic leopard cat), Lynx lynx (lynx), Puma electrophoresis, allozyme data, karyology, endogenous concolor (puma), and Acinonyx jubatus (cheetah) were retroviruses, mitochondrial (mt) DNA sequences, sex included. In addition, two representatives of the domes- chromosomes-linked genes, and chemical signals (Bin- tic cat lineage and one outgroup taxa from family Viv- inda-Emonds, 2001; Collier and O’Brien, 1985; Johnson erridae or Hyaenidae were also utilized. Taxonomic and O’Brien, 1997; Lopez et al., 1994; O’Brien et al., classiWcation of cat species followed Nowak (1999). 1987; Pecon Slattery and O’Brien, 1998; Reeves and Total genomic DNA was isolated from blood, frozen or O’Brien, 1984). However, little prior research focused hair tissues based on the method of Sambrook et al. nuclear genes at the DNA level. In the present paper, the (1989) and prepared for subsequent polymerase chain seventh intron of the single-copy Wbrinogen gene reaction (PCR). (-chain; -Wbrinogen intron 7) from the nuclear genome Two felid-speciWc primers FGB-FelF and FGB-FelR was used for phylogenetic resolution among closely (Table 2) used to amplify -Wbrinogen intron 7 related pantherine cats. The utility of this gene segment (t650 bp) were designed from conserved regions in has been successfully explored at diVerent taxonomic Xanking exons, based on the homologous comparisons levels in studies of birds (Johnson and Clayton, 2000; of available -Wbrinogen sequences for birds (Prychitko Moyle, 2004; Prychitko and Moore, 1997, 2000, 2003; and Moore, 1997), human (Chung et al., 1983), and rat Weibel and Moore, 2002) and reptiles (Creer et al., 2003; (Eastman and Gilula, 1989). MtDNA PCR products Giannasi et al., 2001), however, still lacking in those of were obtained using ND2-FelF/ND2-FelR primer pair mammals. Our work is the Wrst to explore the potential for ND2 (1038 bp), as well as ND4-FelF/ND4-FelR of -Wbrinogen intron 7 as a genetic marker in carnivo- primer pair for ND4 (1368 bp). Additional internal ran systematics. We also sequenced two large complete primers for amplifying these three genes (Table 2) were NADH dehydrogenase (ND2 and ND4) genes from mt also synthesized. The optimal conditions adopted in genome, given the general thought that analysis of multi- PCRs were 95 °C initial hot start for 5 min, 35 cycles of ple independently inherited genes is especially eVective in 94 °C denaturation for 1 min, 50–56 °C annealing for testing for congruence and estimating organismal phy- 1 min, and 72 °C extension for 1 min. logeny and, in addition, our previously reported nuclear With above-mentioned primers, three new target seg- interphotoreceptor retinoid-binding protein (IRBP) and ments for each sample were acquired in almost all cases transthyretin (TTR) genes (Yu et al., 2004b), together except an incomplete ND2 sequence (683 bp) from P. with four other available mtDNA characters (12SrRNA, uncia (snow leopard) due to sequencing diYculty in one cytochrome b, 16SrRNA, and ND5 genes; Janczewski end of the gene, as well as unavailable -Wbrinogen et al., 1995; Johnson and O’Brien, 1997; Masuda et al., intron 7 sequences from P. onca (jaguar) and Puma con- 1996) for the same set of cat species were also added to color (puma) because of insuYcient template content in the present analyses. hair tissues as well as from Acinonyx jubatus (cheetah) Sequence data from 9 genes (three nuclear and six mt) because of the absence of sample. These three taxa were of 12 pantherine cats and 2 domestic cats was analyzed, thus only represented in the mtDNA datasets. ND2 and separately or in a variety of combinations here, with a ND4 sequences for Felis catus (domestic cat) and Acin- view of (1) providing a broader understanding of inter- onyx jubatus (cheetah) were directly retrieved from Gen- speciWc relationships within the pantherine group, (2) Bank. In all, 34 out of 40 ingroup sequences were assessing the utility of -Wbrinogen intron 7 as a novel produced in this study. marker in carnivoran phylogenetics, and (3) comparing evolutionary patterns of diVerent genes and their values 2.2. Sequencing and data analysis for resolution of low level feline questions. The ampliWed PCR products were puriWed and sequenced in both directions with an ABI automated 2. Materials and methods sequencer. Acquired sequences were submitted to Gen- Bank for BLAST searching (Altschul et al., 1997) to ver- 2.1. DNA samples and PCR ampliWcations ify the data. New GenBank Accession Nos. are given in Table 1. Fourteen felids in the family Felidae were examined Separate alignments of -Wbrinogen intron 7 (from 11 and listed in Table 1. All the Wve currently recognized ingroup) and two mtDNA (ND2 and ND4; from 14 members of genus Panthera in the pantherine lineage, ingroup) sequences data were conducted with CLUS- including P. leo (lion), P. tigris (tiger), P. pardus (leop- TAL X program (Thompson et al., 1997) and reWned by ard), P. onca (jaguar), and P. uncia (snow leopard), and visual inspection. Protein-coding mtDNA alignments seven other pantherine cats, including Neofelis nebulosa were straightforward while the -Wbrinogen intron 7 (clouded leopard), Otocolobus manul (Pallas’s cat), Prof- alignment exhibited obvious sequence length variation. Table 1 List of taxonomic samples and sequences used in this study Taxon Newly established datasets Previously available datasets L. Yu, Y.-p. Zhang / Molecular Phylogenetics and Evolution 35 (2005) 483–495 ScientiWc nameA Common name Sample source Nuclear gene Mitochondrial genes Nuclear gene Mitochondrial genesC -Fibrinogen ND2 ND4 IRBP exon TTR intron 16SrRNA ND5 intron Pantherine
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